Abstract
This study describes early immunological mechanisms that underlie resistance to Teladorsagia circumcincta infection in adult Churra sheep. After a first experimental infection, 6 animals were classified as resistant (RG) and 6 as susceptible (SG) to T. circumcincta infection based on their cumulative faecal egg count (cFEC) at the end of the infection. RG showed higher IgA levels against somatic antigen of T. circumcincta fourth-larvae stage (L4) in serum at day 3 post-infection (pi) (p < 0.05) and close to significance at day 21 pi (p = 0.06). Moreover, a strong negative correlation between cFEC and specific IgA was only significant in RG at day 3 pi (r = − 0.870; p < 0.05), but absent in SG. At the end of this infection, sheep were treated with moxidectin and infected again 3 weeks later to be slaughtered at day 7 pi. At necropsy, the specific IgA levels in gastric mucosa were similar between groups; the absence differences at day 7 pi could be due to a previous increase in the IgA response, probably around day 3 pi, as described during the first infection. L4 burden, 68% lower in RG than in SG, was influenced by the specific IgA in gastric mucus and the number of γδ T cells. RG group showed a positive correlation between γδ T cells and eosinophils (r = 0.900; p = 0.037); however, this correlation was not found in SG. These results show that these two phenotypes show different early immune response pattern to T. circumcincta infection in Churra sheep.
Data availability
Data will be available on https://www.re3data.org/ after manuscript acceptance.
References
Armour J, Jarrett WFH, Jennings FW (1996) Experimental Ostertagia circumcincta infections in sheep: development and pathogenesis of a single infection. Am J Vet Res 27:1267–1278
Atlija M, Prada JM, Gutiérrez-Gil B, Rojo-Vázquez FA, Stear MJ, Arranz JJ, Martínez-Valladares M (2016) Implementation of an extended ZINB model in the study of low levels of natural gastrointestinal nematode infections in adult sheep. BMC Vet Res 12:1–9. https://doi.org/10.1186/s12917-016-0723-7
Burgess CGS, Bartley Y, Redman E, Skuce PJ, Nath M, Whitelaw F, Tait A, Gilleard JS, Jackson F (2012) A survey of the trichostrongylid nematode species present on UK sheep farms and associated anthelmintic control practices. Vet Parasitol 189:299–307. https://doi.org/10.1016/j.vetpar.2012.04.009
Chitneedi PK, Suárez-Vega A, Martínez-Valladares M, Arranz JJ, Gutiérrez-Gil B (2018) Exploring the mechanisms of resistance to Teladorsagia circumcincta infection in sheep through transcriptome analysis of abomasal mucosa and abomasal lymph nodes. Vet Res 49:1–11. https://doi.org/10.1186/s13567-018-0534-x
González JF, Hernández Á, Meeusen ENT, Rodríguez F, Molina JM, Jaber JR, Raadsma HW, Piedrafita D (2011) Fecundity in adult Haemonchus contortus parasites is correlated with abomasal tissue eosinophils and γδ T cells in resistant Canaria hair breed sheep. Vet Parasitol 178:286–292. https://doi.org/10.1016/j.vetpar.2011.01.005
Gunia M, Phocas F, Gourdine JL, Bijma P, Mandonnet N (2013) Simulated selection responses for breeding programs including resistance and resilience to parasites in creole goats. J Anim Sci 91:572–581. https://doi.org/10.2527/jas.2011-5071
Halliday AM, Morrison WI, Smith WD (2009) Kinetics of the local cellular response in the gastric lymph of immune and susceptible sheep to infection with Teladorsagia circumcincta. Parasite Immunol 31:402–411. https://doi.org/10.1111/j.1365-3024.2009.01119.x
Hamel D, Bosco A, Rinaldi L, Cringoli G, Kaulfuß KH, Kellermann M, Fischer J, Wang H, Kley K, Mayr S, Rauh R, Visser M, Wiefel T, Fankhauser B, Rehbein S (2017) Eprinomectin pour-on (EPRINEX® Pour-on, Merial): efficacy against gastrointestinal and pulmonary nematodes and pharmacokinetics in sheep. BMC Vet Res 13:1–12. https://doi.org/10.1186/s12917-017-1075-7
Hernández JN, Meeusen E, Stear M, Rodríguez F, Piedrafita D, González JF (2017) Modulation of Haemonchus contortus infection by depletion of γδ+ T cells in parasite resistant Canaria hair breed sheep. Vet Parasitol 237:57–62. https://doi.org/10.1016/j.vetpar.2017.02.021
Martínez-Valladares M, Vara-Del Río MP, Cruz-Rojo MA, Rojo-Vázquez FA (2005) Genetic resistance to Teladorsagia circumcincta: IgA and parameters at slaughter in Churra sheep. Parasite Immunol 27:213–218. https://doi.org/10.1111/j.1365-3024.2005.00769.x
Martínez-Valladares M, Geurden T, Bartram DJ, Martínez-Pérez JM, Robles-Pérez D, Bohórquez A, Florez E, Meana A, Rojo-Vázquez FA (2015) Resistance of gastrointestinal nematodes to the most commonly used anthelmintics in sheep, cattle and horses in Spain. Vet Parasitol 211:228–233. https://doi.org/10.1016/j.vetpar.2015.05.024
McNeilly TN, Rocchi M, Bartley Y et al (2013) Suppression of ovine lymphocyte activation by Teladorsagia circumcincta larval excretory-secretory products. Vet Res 44:1. https://doi.org/10.1186/1297-9716-44-70
McRae KM, Good B, Hanrahan JP et al (2014) Response to Teladorsagia circumcincta infection in Scottish Blackface lambs with divergent phenotypes for nematode resistance. Vet Parasitol 206:200–207. https://doi.org/10.1016/J.VETPAR.2014.10.023
McRae KM, Good B, Hanrahan JP et al (2016) Transcriptional profiling of the ovine abomasal lymph node reveals a role for timing of the immune response in gastrointestinal nematode resistance. Vet Parasitol 224:96–108. https://doi.org/10.1016/j.vetpar.2016.05.014
Nagata WB, da Cruz Panegossi MF, Bresciani KDS, Gomes JF, Kaneto CN, Perri SHV (2019) Resistance of gastrointestinal nematodes to five different active principles in sheep infected naturally in São Paulo State, Brazil. Small Rumin Res 172:48–50. https://doi.org/10.1016/j.smallrumres.2018.10.001
Nisbet AJ, Meeusen EN, González JF, Piedrafita DM (2016) Immunity to Haemonchus contortus and vaccine development. Adv Parasitol 93:353–396. https://doi.org/10.1016/bs.apar.2016.02.011
Notter DR, Burke JM, Miller JE, Morgan JLM (2017) Factors affecting fecal egg counts in periparturient Katahdin ewes and their lambs. J Anim Sci 95:103–112. https://doi.org/10.2527/jas2016.0955
Palomo-Couoh JG, Aguilar-Caballero AJ, Torres-Acosta JF d J, Magaña-Monforte JG (2016) Evaluation of different models to segregate Pelibuey and Katahdin ewes into resistant or susceptible to gastrointestinal nematodes. Trop Anim Health Prod 48:1517–1524. https://doi.org/10.1007/s11250-016-1122-6
Preston S, Piedrafita D, Sandeman M, Cotton S (2019) The current status of anthelmintic resistance in a temperate region of Australia; implications for small ruminant farm management. Vet Parasitol Reg Stud Reports 17:100313. https://doi.org/10.1016/j.vprsr.2019.100313
Robinson N, Piedrafita D, Snibson K, Harrison P, Meeusen EN (2010) Immune cell kinetics in the ovine abomasal mucosa following hyperimmunization and challenge with Haemonchus contortus. Vet Res 41:1–10. https://doi.org/10.1051/vetres/2010009
Strain SAJ, Stear MJ (1999) The recognition of molecules from fourth-stage larvae of Ostertagia circumcincta by IgA from infected sheep. Parasite Immunol 21:163–168. https://doi.org/10.1046/j.1365-3024.1999.00225.x
Traversa D, von Samson-Himmelstjerna G (2016) Anthelmintic resistance in sheep gastro-intestinal strongyles in Europe. Small Rumin Res 135:75–80. https://doi.org/10.1016/j.smallrumres.2015.12.014
Zaragoza-Vera CV, Aguilar-Caballero AJ, González-Garduño R, Arjona-Jiménez G, Zaragoza-Vera M, Torres-Acosta JFJ, Medina-Reynés JU, Berumen-Alatorre AC (2019) Variation in phenotypic resistance to gastrointestinal nematodes in hair sheep in the humid tropics of Mexico. Parasitol Res 118:567–573. https://doi.org/10.1007/s00436-018-06201-w
Acknowledgements
WC1 antibody (clone 19.19) was generously ceded by Dr. David Piedrafita (Federation University, Australia).
Funding
Financial support for this project was received from the LE248U14 project of Junta de Castilla and León Government. VCGA is funded by Junta de Castilla y León and FSE (LE082-18), EVG by FPU grant (FPU17/00627) from Spanish Ministry of Education, BGG by the “Ramón y Cajal” Programme (RYC-2012-10230) from the Spanish Ministry of Economy, Industry and Competitiveness (MINECO), MMV by the “Ramón y Cajal” Programme (RYC-2015-18368) from the Spanish Ministry of Economy, Industry and Competitiveness (MINECO) and JNH by Agencia Canaria de Investigación, Innovación y Sociedad de la Información del Gobierno de Canarias y Fondo Social Europeo (ProID2017010109).
Author information
Authors and Affiliations
Contributions
Conceptualization, BGG, JJA, MMV; methodology, VCG, JFG, JNH, EVG, MMV; drafting the manuscript VCG, FRV, MMV; reviewer the manuscript all authors; validation FRV, JJA, BGG; resources, MMV; funding acquisition BGG; experimental design, BGG, JJA, MMV. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
This study was carried out according to the National Spanish legislation on the protection of animals used in experimentation (Royal Decree 53/2013), after the approval of the competent body, Junta de Castilla y León.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Abdul Jabbar
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Castilla-Gómez de Agüero, V., González, J.F., Hernández, J.N. et al. Differences within Churra breed sheep in the early immune response to the infection by Teladorsagia circumcincta. Parasitol Res 120, 1115–1120 (2021). https://doi.org/10.1007/s00436-020-06953-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-020-06953-4